Mismatch between cuticle deposition and area expansion in fruit skins allows potentially catastrophic buildup of elastic strain

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Xiaoting Lai
  • Bishnu Prasad Khanal
  • Moritz Knoche
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Details

Original languageEnglish
Pages (from-to)1145-1156
Number of pages12
JournalPLANTA
Volume244
Issue number5
Early online date28 Jul 2016
Publication statusPublished - 1 Nov 2016

Abstract

Main conclusion: The continuous deposition of cutin and wax during leaf and fruit growth is crucial to alleviate elastic strain of the cuticle, minimizethe risk of failure and maintain its barrier functions. The cuticular membrane (CM) is a lipoidal biopolymer that covers primary surfaces of terrestrial plants. CMs have barrier functions in water and solute transfer and pathogen invasion. These require intact CMs throughout growth. This is a challenge particularly for fruit, because they increase in area from initiation through to maturity. Our paper investigates the effects of cutin and wax deposition on strain buildup in the CM. We use developing fruits and leaves of apple (Malus × domestica) and sweet cherry (Prunus avium) as models. The hypothesis was that the continuous deposition of the CM prevents the buildup of excessive elastic strain in fruit and leaves. Strains were quantified from decreases in surface area of CMs after isolation from epidermal discs, after wax extraction and from increases in surface area during development. Cuticle mass per unit area increased throughout development in apple fruit, and leaves of apple and sweet cherry. In sweet cherry fruit, however, CM mass increased only initially, but thereafter decreased as the surface expanded rapidly. The release of strain on CM isolation was low in apple fruit and leaves and sweet cherry leaves, but high in sweet cherry fruit. Conversely, strains fixed by the deposition of wax and cutin were high in apple fruit and leaves and sweet cherry leaves, but low in sweet cherry fruit. Our results indicate that in expanding organs, deposition of cutin and wax in the CM allows conversion of elastic to plastic strain. Hence, any lack of such deposition allows buildup of high, potentially catastrophic, elastic strain.

Keywords

    Apple, Cherry, Cutin, Rheology, Stress, Wax

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Genetics
  • Agricultural and Biological Sciences(all)
  • Plant Science

Cite this

Mismatch between cuticle deposition and area expansion in fruit skins allows potentially catastrophic buildup of elastic strain. / Lai, Xiaoting; Khanal, Bishnu Prasad; Knoche, Moritz.
In: PLANTA, Vol. 244, No. 5, 01.11.2016, p. 1145-1156.

Research output: Contribution to journalArticleResearchpeer review

Lai X, Khanal BP, Knoche M. Mismatch between cuticle deposition and area expansion in fruit skins allows potentially catastrophic buildup of elastic strain. PLANTA. 2016 Nov 1;244(5):1145-1156. Epub 2016 Jul 28. doi: 10.1007/s00425-016-2572-9
Lai, Xiaoting ; Khanal, Bishnu Prasad ; Knoche, Moritz. / Mismatch between cuticle deposition and area expansion in fruit skins allows potentially catastrophic buildup of elastic strain. In: PLANTA. 2016 ; Vol. 244, No. 5. pp. 1145-1156.
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abstract = "Main conclusion: The continuous deposition of cutin and wax during leaf and fruit growth is crucial to alleviate elastic strain of the cuticle, minimizethe risk of failure and maintain its barrier functions. The cuticular membrane (CM) is a lipoidal biopolymer that covers primary surfaces of terrestrial plants. CMs have barrier functions in water and solute transfer and pathogen invasion. These require intact CMs throughout growth. This is a challenge particularly for fruit, because they increase in area from initiation through to maturity. Our paper investigates the effects of cutin and wax deposition on strain buildup in the CM. We use developing fruits and leaves of apple (Malus × domestica) and sweet cherry (Prunus avium) as models. The hypothesis was that the continuous deposition of the CM prevents the buildup of excessive elastic strain in fruit and leaves. Strains were quantified from decreases in surface area of CMs after isolation from epidermal discs, after wax extraction and from increases in surface area during development. Cuticle mass per unit area increased throughout development in apple fruit, and leaves of apple and sweet cherry. In sweet cherry fruit, however, CM mass increased only initially, but thereafter decreased as the surface expanded rapidly. The release of strain on CM isolation was low in apple fruit and leaves and sweet cherry leaves, but high in sweet cherry fruit. Conversely, strains fixed by the deposition of wax and cutin were high in apple fruit and leaves and sweet cherry leaves, but low in sweet cherry fruit. Our results indicate that in expanding organs, deposition of cutin and wax in the CM allows conversion of elastic to plastic strain. Hence, any lack of such deposition allows buildup of high, potentially catastrophic, elastic strain.",
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AU - Khanal, Bishnu Prasad

AU - Knoche, Moritz

N1 - Funding Information: We thank Dr. Sandy Lang for his very thoughtful comments when reviewing an earlier version of this manuscript. We also thank the German Science Foundation (DFG) for funding part of this research. Thank you.

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AB - Main conclusion: The continuous deposition of cutin and wax during leaf and fruit growth is crucial to alleviate elastic strain of the cuticle, minimizethe risk of failure and maintain its barrier functions. The cuticular membrane (CM) is a lipoidal biopolymer that covers primary surfaces of terrestrial plants. CMs have barrier functions in water and solute transfer and pathogen invasion. These require intact CMs throughout growth. This is a challenge particularly for fruit, because they increase in area from initiation through to maturity. Our paper investigates the effects of cutin and wax deposition on strain buildup in the CM. We use developing fruits and leaves of apple (Malus × domestica) and sweet cherry (Prunus avium) as models. The hypothesis was that the continuous deposition of the CM prevents the buildup of excessive elastic strain in fruit and leaves. Strains were quantified from decreases in surface area of CMs after isolation from epidermal discs, after wax extraction and from increases in surface area during development. Cuticle mass per unit area increased throughout development in apple fruit, and leaves of apple and sweet cherry. In sweet cherry fruit, however, CM mass increased only initially, but thereafter decreased as the surface expanded rapidly. The release of strain on CM isolation was low in apple fruit and leaves and sweet cherry leaves, but high in sweet cherry fruit. Conversely, strains fixed by the deposition of wax and cutin were high in apple fruit and leaves and sweet cherry leaves, but low in sweet cherry fruit. Our results indicate that in expanding organs, deposition of cutin and wax in the CM allows conversion of elastic to plastic strain. Hence, any lack of such deposition allows buildup of high, potentially catastrophic, elastic strain.

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